1887

Abstract

RD-114 virus is a replication-competent feline endogenous retrovirus (ERV). RD-114 virus had been thought to be xenotropic; however, recent findings indicate that RD-114 virus is polytropic and can infect and grow efficiently in feline cells. Receptor(s) for RD-114 virus has not been identified and characterized in cats. In this study, we confirmed that two feline sodium-dependent neutral amino acid transporters (ASCTs), fASCT1 and fASCT2, function as RD-114 virus receptors. By chimeric analyses of feline and murine ASCTs, we revealed that extracellular loop 2 of both fASCT1 and fASCT2 determines the susceptibility to RD-114 virus. Further, we revealed ubiquitous expression of these genes, consistent with the general metabolic role of the ASCT molecules. Our study indicates that RD-114 virus may reinfect tissues and cells in cats, once the virus is activated. Implications of the involvement of RD-114 virus in feline oncogenesis are also discussed.

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2013-07-01
2020-04-04
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References

  1. Arriza J. L., Kavanaugh M. P., Fairman W. A., Wu Y. N., Murdoch G. H., North R. A., Amara S. G. 1993; Cloning and expression of a human neutral amino acid transporter with structural similarity to the glutamate transporter gene family. J Biol Chem 268:15329–15332[PubMed]
    [Google Scholar]
  2. Cheney C. M., Rojko J. L., Kociba G. J., Wellman M. L., Di Bartola S. P., Rezanka L. J., Forman L., Mathes L. E. 1990; A feline large granular lymphoma and its derived cell line. In Vitro Cell Dev Biol 26:455–463 [CrossRef][PubMed]
    [Google Scholar]
  3. Dunn K. J., Yuan C. C., Blair D. G. 1993; A phenotypic host range alteration determines RD114 virus restriction in feline embryonic cells. J Virol 67:4704–4711[PubMed]
    [Google Scholar]
  4. Fischinger P. J., Peebles P. T., Nomura S., Haapala D. K. 1973; Isolation of RD-114-like oncornavirus from a cat cell line. J Virol 11:978–985[PubMed]
    [Google Scholar]
  5. Gifford R., Tristem M. 2003; The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26:291–315 [CrossRef][PubMed]
    [Google Scholar]
  6. Hartley J. W., Wolford N. K., Old L. J., Rowe W. P. 1977; A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A 74:789–792 [CrossRef][PubMed]
    [Google Scholar]
  7. Kessler Y., Helfer-Hungerbuehler A. K., Cattori V., Meli M. L., Zellweger B., Ossent P., Riond B., Reusch C. E., Lutz H., Hofmann-Lehmann R. 2009; Quantitative TaqMan real-time PCR assays for gene expression normalisation in feline tissues. BMC Mol Biol 10:106 [CrossRef][PubMed]
    [Google Scholar]
  8. Koo H. M., Parthasarathi S., Ron Y., Dougherty J. P. 1994; Pseudotyped REV/SRV retroviruses reveal restrictions to infection and host range within members of the same receptor interference group. Virology 205:345–351 [CrossRef][PubMed]
    [Google Scholar]
  9. Kyte J., Doolittle R. F. 1982; A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132 [CrossRef][PubMed]
    [Google Scholar]
  10. Louwerens M., London C. A., Pedersen N. C., Lyons L. A. 2005; Feline lymphoma in the post-feline leukemia virus era. J Vet Intern Med 19:329–335[PubMed]
    [Google Scholar]
  11. Marin M., Tailor C. S., Nouri A., Kabat D. 2000; Sodium-dependent neutral amino acid transporter type 1 is an auxiliary receptor for baboon endogenous retrovirus. J Virol 74:8085–8093 [CrossRef][PubMed]
    [Google Scholar]
  12. Marin M., Lavillette D., Kelly S. M., Kabat D. 2003; N-linked glycosylation and sequence changes in a critical negative control region of the ASCT1 and ASCT2 neutral amino acid transporters determine their retroviral receptor functions. J Virol 77:2936–2945 [CrossRef][PubMed]
    [Google Scholar]
  13. McGrath M. S., Weissman I. L. 1979; AKR leukemogenesis: identification and biological significance of thymic lymphoma receptors for AKR retroviruses. Cell 17:65–75 [CrossRef][PubMed]
    [Google Scholar]
  14. Miyazawa T. 2010; Endogenous retroviruses as potential hazards for vaccines. Biologicals 38:371–376 [CrossRef][PubMed]
    [Google Scholar]
  15. Miyazawa T., Yoshikawa R., Golder M., Okada M., Stewart H., Palmarini M. 2010; Isolation of an infectious endogenous retrovirus in a proportion of live attenuated vaccines for pets. J Virol 84:3690–3694 [CrossRef][PubMed]
    [Google Scholar]
  16. Narushima R., Shimazaki T., Takahashi T. 2011; Development of a real-time reverse-transcription-PCR method for detection of RD114 virus in canine vaccines. Biologicals 39:89–93 [CrossRef][PubMed]
    [Google Scholar]
  17. Narushima R., Usui T., Ogawa T., Shimazaki T. 2010; Detection of infectious RD114 virus in feline live multivalent vaccines and provisional safety evaluation in cats. J Jpn Vet Med Assoc 63:630–633 (in Japanese with English summary)
    [Google Scholar]
  18. Niman H. L., Stephenson J. R., Gardner M. B., Roy-Burman P. 1977; RD-114 and feline leukaemia virus genome expression in natural lymphomas of domestic cats. Nature 266:357–360 [CrossRef][PubMed]
    [Google Scholar]
  19. Okada M., Yoshikawa R., Shojima T., Baba K., Miyazawa T. 2011; Susceptibility and production of a feline endogenous retrovirus (RD-114 virus) in various feline cell lines. Virus Res 155:268–273 [CrossRef][PubMed]
    [Google Scholar]
  20. Rasko J. E., Battini J. L., Gottschalk R. J., Mazo I., Miller A. D. 1999; The RD114/simian type D retrovirus receptor is a neutral amino acid transporter. Proc Natl Acad Sci U S A 96:2129–2134[PubMed] [CrossRef]
    [Google Scholar]
  21. Reeves R. H., O’Brien S. J. 1984; Molecular genetic characterization of the RD-114 gene family of endogenous feline retroviral sequences. J Virol 52:164–171[PubMed]
    [Google Scholar]
  22. Sakaguchi S., Okada M., Shojima T., Baba K., Miyazawa T. 2008; Establishment of a LacZ marker rescue assay to detect infectious RD114 virus. J Vet Med Sci 70:785–790 [CrossRef][PubMed]
    [Google Scholar]
  23. Tailor C. S., Nouri A., Zhao Y., Takeuchi Y., Kabat D. 1999; A sodium-dependent neutral-amino-acid transporter mediates infections of feline and baboon endogenous retroviruses and simian type D retroviruses. J Virol 73:4470–4474 [CrossRef][PubMed]
    [Google Scholar]
  24. Takeuchi Y., Patience C., Magre S., Weiss R. A., Banerjee P. T., Le Tissier P., Stoye J. P. 1998; Host range and interference studies of three classes of pig endogenous retrovirus. J Virol 72:9986–9991[PubMed]
    [Google Scholar]
  25. Teich N. 1984; Taxonomy of retroviruses. In RNA Tumor Viruses pp. 25–208 Edited by Weiss R., Teich N., Varmus H., Coffin J. New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  26. Teske E., van Straten G., van Noort R., Rutteman G. R. 2002; Chemotherapy with cyclophosphamide, vincristine, and prednisolone (COP) in cats with malignant lymphoma: new results with an old protocol. J Vet Intern Med 16:179–186 [CrossRef][PubMed]
    [Google Scholar]
  27. Utsunomiya-Tate N., Endou H., Kanai Y. 1996; Cloning and functional characterization of a system ASC-like Na+-dependent neutral amino acid transporter. J Biol Chem 271:14883–14890 [CrossRef][PubMed]
    [Google Scholar]
  28. Yoshikawa R., Sato E., Igarashi T., Miyazawa T. 2010; Characterization of RD-114 virus isolated from a commercial canine vaccine manufactured using CRFK cells. J Clin Microbiol 48:3366–3369 [CrossRef][PubMed]
    [Google Scholar]
  29. Yoshikawa R., Sato E., Miyazawa T. 2011; Contamination of infectious RD-114 virus in vaccines produced using non-feline cell lines. Biologicals 39:33–37 [CrossRef][PubMed]
    [Google Scholar]
  30. Yoshikawa R., Sato E., Miyazawa T. 2012a; Presence of infectious RD-114 virus in a proportion of canine parvovirus isolates. J Vet Med Sci 74:347–350 [CrossRef][PubMed]
    [Google Scholar]
  31. Yoshikawa R., Yasuda J., Kobayashi T., Miyazawa T. 2012b; Canine ASCT1 and ASCT2 are functional receptors for RD-114 virus in dogs. J Gen Virol 93:603–607 [CrossRef][PubMed]
    [Google Scholar]
  32. Young G. R., Eksmond U., Salcedo R., Alexopoulou L., Stoye J. P., Kassiotis G. 2012; Resurrection of endogenous retroviruses in antibody-deficient mice. Nature 491:774–778[PubMed]
    [Google Scholar]
  33. Yu P., Lübben W., Slomka H., Gebler J., Konert M., Cai C., Neubrandt L., Prazeres da Costa O., Paul S. other authors 2012; Nucleic acid-sensing Toll-like receptors are essential for the control of endogenous retrovirus viremia and ERV-induced tumors. Immunity 37:867–879 [CrossRef][PubMed]
    [Google Scholar]
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